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LE JOURNAL CANADIEN DES SCIENCES NEUROLOGIQUES
Childhood Cerebral Cysticercosis: Clinical Features and Computed Tomographic Findings
in 89 Mexican Children ARTURO L6PEZ-HERNANDEZ and CARMEN GARAIZAR
SUMMARY: Cerebral cysticercosis was studied in 89 Mexican children. These patients were divided into two groups; those with proven diagnosis and those in whom the diagnosis was strongly suspected. The frequency of childhood cysticercosis at autopsy is significantly less than reported in adults from the same environment. Symptoms of initial cerebral invasion by the parasite include headache, fever, vomiting, and seizures. Cerebral edema is observed more frequently in children than in adults, and is the most common cause of intracranial hypertension. The cerebral edema generally is associated with an en-cephalitic syndrome, either a single bout or a chronic course with multiple relapses. Ar-
RESUME: Nous avons etudie la cysticer-cose cerebrale chez 89 enfants mexicains, divises en deux groupes, un premier dont le diagnostic est certain et un second au diagnostic probable. La frequence de cys-ticercose infantile a I'autopsie est signifi-cativement inferieure a celle notee chez les adultes du mime environnement mais il n'existe pas de difference qualitative dans les presentations cliniques aux 2 ages. Les symptomes initiaux d'envahisement par le parasite sont la cephalee, la fievre, les vomissements et les crises comitiales. L'oedeme cerebral, plus frequent chez les enfants, etait la cause la plus commune de I'hypertension intracrdnienne. Le plus fre-quemment I'aspect clinique groupe l'oedeme
From the Neurology Service, National Institute of Pediatrics D.I.F., Mexico D.F., Mexico.
Translated from Spanish by Harvey B. Sarnat, Faculty of Medicine, University of Calgary.
Requests for Reprints to: Dr. A. Lopez H., Servicio de Neurologia, Instituto Nacional de Pediatria D.I.F., Insurgentes Sur 3700-C, Mexico, D.F., Mexico 14410.
terial hypertension, not previously described, was found in two probable cases. The variability of clinical symptomatology thus is great. Symptoms in childhood cerebral cysticercosis may be totally absent, moderate, or severe and ultimately fatal. Computed tomography of the brain is the most useful diagnostic aid, and determines the dynamic neuroradiologic sequence of this disease, since different images appear at each stage to permit its diagnosis. Un-calcified cysticerci may be demonstrated by contrast enhancement if associated with focal cerebral edema; images thus may disappear and reappear in the clinical course of the disease.
cerebral a un syndrome encephalitique a manifestation simple ou repetitive. Nous avons trouve une hypertension arterielle chez deux malades, ce qui etait prealable-ment inconnu. Cependant la variabilite de la presentation clinique est importante. La cysticercose cerebrale infantile peut etre totalement asymptdmatique, moderee ou severe et ultimement fatale. La tomoden-sotometrie cerebrale est le test le plus important car ilpermet des images differentes a chaque etape qui soulignent le diagnostic. Parfois les tests de contrastes permettent, s'il y a oedeme cerebral focal, d'identifier les cysticerci non calcifies. II est done possible de voir certaines images apparaitre et disparaitre au cours de revolution clinique.
In the abundant literature regarding the clinical picture of cerebral cysticercosis, only two reports exist that focus specifically on cerebral cysticercosis in children (De la Torre et al., 1954; Lopez-Hernandez and Cedillo, 1976). The largest published mixed series in Mexico only includes eight children of a total 0M86 cases (Macias Sanchez and Ordonez, 1970) and the largest series published outside Mexico contains only nine children of 450 cases (Dixon and Lipscomb, 1961). It is obvious that cerebral cysticercosis has received less attention in the child than in the adult, and that because of the small number of published cases at this time, the clinical picture has not been well defined. Nevertheless, since the introduction of computed tomography in Mexico in 1976, many cases have been diagnosed that formerly would have gone undetected, so that this technique has greatly broadened our knowledge of the clinical picture in this disease. The purpose of this paper is to present the clinical, radiologic, and laboratory characteristics of 89 cases of cerebral cysticercosis in patients less than 18 years of age.
MATERIAL AND METHODS All cases of cerebral cysticercosis
admitted to the National Institute of Pediatrics D.I.F. during the period from 1 November 1970 to 30 November 1980 were reviewed retrospectively. The patients were divided in two groups, according to the precision with which the diagnosis was determined:
Group 1 (proven cysticercosis) was composed of 29 symptomatic and asymptomatic patients in whom cerebral cysticercosis was proved by surgical excisional biopsy or autopsy.
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THE CANADIAN JOURNAL OF NEUROLOGICAL SCIENCES
Group 2 (probable cysticercosis) was composed of 60 symptomatic and asymptomatic patients in whom the plain roentgenograms of the skull showed calcifications suggestive of cysticercosis; micro nodular calcifications of 5-12 mm in diameter with a radiolucent center (Cardenas and Cardenas, 1962; Dorfsman, 1963; Santin and Vargas, 1966) or computed tomographic images suggestive of cysticercosis, such as radiolucent cysts, or solid annular nodular cysts (Bentson et al., 1977; Rodriguez-Carbajal et al., 1977; Rodriquez et al., 1978; Lamas et al., 1978).
RESULTS AND COMMENTS Tables I to VIII summarize the
results of both groups of patients. Frequency. The frequency of
cysticercosis of Mexico has been estimated on the basis of a seroepide-miologic study carried out in a representative sample of the general population, which demonstrated that almost 1% of the population had positive serologic reactions (Flisser, 1980), but this study does not address the childhood population. With respect to the frequency of cysticercosis estimated in postmortem studies during the 10 year period in which the study was carried out, 18 cases of a total of 3,000 autopsies were found, giving a percentage of 0.60%. Another pediatric series reported a frequency of 0.14% in 2,900 autopsies (Salas, 1971). These figures are significantly less than those reported in series of adults that vary from 3.6% (maximum) to 1.03% (minimum) in several general hospitals in Mexico City (Costero, 1946;
Martinez et al.i 1975). These figures suggest that the frequency of childhood cerebral cysticercosis is less than that of the adult, and the reports of other authors substantiate this view. In Chile, Schenone et al. (1973) found 2 cases among 27,338 unselected autopsies of children, an incidence of 0.007%, and 89 cases among 104,854 autopsies in adults, a yield of 2.39%. In Costa Rica, Piza et al. (1967) found no cases among 4,700 autopsies of children under 7 years of age, while in adults the incidence was 0.5%.
Age and Sex. As indicated in Table I, the majority of cases, 90.9% are grouped between 6 and 18 years of age. Only 8 cases (9.1%) occurred in children 5 years of age or less.
The youngest child in our series is 11 months, and the youngest reported in the literature is 5 days (Lopez, 1943).
TABLE I: Distribution of Age and Sex
AGE (years) 0- 5 5-10
10- 15 15- 18
Group 1 2 9 6 1
18
FEMALE Group 2
2 12 18 4
36
Total 4
21 24
5 54 (60.6%)
Group 1 4 3 2 2
11
MALE Group 2
0 9 7 8
24
Total 4
12 9
10 35 (39.4%)
Total 8( 9.1%)
33 (37.0%) 33 (37.0%) 15(16.9%)
89 (100%)
TABLE II: Clinical Manifestations of Cerebral Cysticercosis
SYMPTOMS
Symptomatic Intracranial hypertension Seizures Alteration of stretch
reflexes Visual impairment Alterations of cranial nerves Impairment of consciousness Impaired coordination Psychotic reactions Meningeal signs Somatic paralysis Mental deterioration Asymptomatic
GROUP 1 Number of Cases
16 16 12
13 9
10 9 8 6 6 3 3
13
Percent
100 75
81 56 62 56 50 37 37 18 18
GROUP2 Number of Cases
58 25 48
13 11 8 1 9 3 2 6 9 2
Percent
43 82
22 18 13 1.7
15.5 5.1 3.4
10.2 15.5
TOTAL Number of Cases
74 41 60
26 20 18 10 17 9 8 9
12 15
Percent 83.2 55 81
35 27 24 13 22 12 10.8 12 16 16.8
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LE JOURNAL CANADIEN DES SCIENCES NEUROLOGIQUES
Although a 60% predominance of females was found in our series, this difference does not appear to be significant since other authors have found a male predominance (Macias Sanchez and Ordonez, 1970) or have not found significant differences between the sexes (Escobar, 1952; BriseTio et al., 1961).
Clinical Picture. There were significant differences in the clinical manifestations for the two groups of patients (Table II). The first difference is the predominance of asymptomatic patients in Group 1, 44.8%, compared with 3.3% in Group 2. This difference is explained by the fact that the cases in Group 1 were discovered at autopsy while those in Group 2 were identified as an incidental finding on a radiograph of the skull or face taken to investigate non-neurologic symptoms. The second difference was the predominance of increased intracranial pressure in symptomatic patients -100% of the cases in Group 1 contrasted with 43% in Group 2. When the chi-square test was applied, this difference was statistically significant (p<0.05). The second most frequent symptom, epilepsy, was present in 82% of Group 2 cases compared with 75% of Group 1, but this difference was not statistically significant (p>0.05). These figures suggest that the most frequent clinical manifestation of childhood cysticercosis in proven cases is intracranial hypertension, a feature previously demonstrated in adults (Briseno et al., 1961; Zenteno et al., 1961; Lombardo and Mateos, 1961). The method of selection influences the result; when the non-proven cases are
Generalized tonic-clonic Partial with elementary
symptomatology Partial with complex
symptomatology Generalized, simple absence More than one type of seizure
TOTAL
Lopez-Hernandez & Garaizar
analyzed, intracranial hypertension is not as frequent. Nevertheless, a basic difference exists between the mechanisms for intracranial hypertension in children and adults. In adults, the majority of cases are accompanied by hydrocephalus. Macias Sanchez and OdorTez (1970) determined the size of the ventricles in 75 cases. They found hydrocephalus in 56 and normal sized ventricles in 14 of these cases. Zenteno et al. (1961) reported a series of 30 adult patients, 29 with hydrocephalus and 1 with normal ventricles. Lombardo and Mateos (1961) reported 22 adult cases, 18 of whom presented with dilated ventricles. The mechanism by which hydrocephalus is produced in cysticercosis is fundamentally mechanical due to inflammation and obstruction at the basal cisterns and/or within the ventricular system (Rabiela et al., 1979). In our series, the frequency of hydrocephalus was significantly lower, since of a total of 41 cases of intracranial hypertension, only 13 had ventricular dilatation and 27 exhibited normal or collapsed ventricles. This finding suggests that cerebral edema is more frequent than hydrocephalus as a cause of increased i n t r a c r a n i a l p r e s s u r e . T h e predominance of cerebral edema in infancy also has been observed by Ste-pien (1962). We propose the term 'cysticercus encephalitis' to denote the clinical picture of cerebral edema, intracranial hypertension, and multiple encephalitic symptoms, as seen during the course of some of these patients. Arterial hypertension was found in two cases, probably related to increased intracranial pressure.
TABLE III: Types of Seizures
GROUP 1 Number of Cases Percent
8 66.6
6 50.0
1 8.3
0 0 3 25.0
12
Neither in the literature reviewed nor in our autopsy series were childhood cases of spinal cysticercosis found, despite the frequency of this entity in adults (Cabieses et al., 1959; Testa, 1965; Hesketh, 1965; Trelles et al., 1970; Carmalt et al., 1975; Queiroz, 1975; Garza-Mercado, 1976; Natara-jan et al., 1976; Roy et al, 1976; Kur-rein and Vickers, 1977; Firemark, 1978; Akiguchi et al., 1979). Finally it is noteworthy that we have found a common association of cysticercosis with other entities, such as brain tumors, lupus erythematosis, leukemia, salmonellosis, etc., in the autopsied cases. The clinician should be careful to not dismiss cerebral cysticercosis as a diagnosis simply because symptoms and signs of another entity are present.
Types of Seizures. The variety of seizure most frequently encountered was the generalized tonic-clonic type, with no significant difference between the two groups (Table III).
Clinical Evolution. Table IV demonstrates that as in adults, the clinical course of cysticercosis is quite variable in childhood. It can follow a totally asymptomatic course or acquire a progressive and serious character leading to a fatal outcome (17.2% mortality in Group 1, 0% mortality in Group 2). There is also an intermediate form, the most frequent of all, represented by the asymptomatic cases of Group 2 which on occasion follow a chronic course (36% with more than 5 years of evolution) and may develop relapses when treatment is discontinued.
Cerebrospinal Fluid (CSF) Findings. As seen in Table V, some cases of
GROUP2 Number of Cases Percent
39 80.8
15 31.9
3 6.3 1 2.12
10 21.2 48
NOVEMBER 1982—403
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THE CANADIAN JOURNAL OF NEUROLOGICAL SCIENCES
Asymptomatic Symptomatic Mortality Relapses following treatment
More than 5 years of evolution
Normal CSF Abnormal CSF Increased protein Pleocytosis Eosinophilia Decreased glucose
TOTAL
Normal Intracranial hypertension Intracranial calcifications
TABLE IV: Clinical Evolution
GROUP 1 Number of Cases
13 16 5 6 3
Percent 44.8 55.2 17.2 34.0 10.3
GROUP 2 Number of Cases
2 58
0 8
21
TABLE V: Cerebrospinal Fluid (CSF) Findings
GROUP 1 Number of Cases
5 13 9
12 3 4
18
Findings in
Percent 27.7 72.2
TABLE VI
Roentgenogram
GROUP 1 Number of Cases
6 9 3
Percent 35.2 52.9 17.6
Percent 3.3
96.7 0
13 36
GROUP2 Number of Cases
17 10 5
10 4 0
27
m of Skull
Percent 62.9 37.0
GROUP 2 Number of Cases
6 13 44
Percent 10 21.6 73.3
TOTAL 15 74
5 14 24
Percent 16.8 83.2
5.6 15.7 26.9
TOTAL Number of Cases
22 23 14 22
7 4
Percent 48.8 51.1 31.1 48.8 15.5 8.8
TOTAL Number of Cases
12 22 47
Percent 13.5 24.7 52.8
cysticercosis did not show any CSF abnormalities. When abnormalities were present, the most frequent was p l eocy tos i s . The presence of eosinophils in the CSF is considered pathognomonic of cysticercosis in Mexico (Hernandez-Peniche et al., 1968), but it is noteworthy that only 7 of the 45 CSF specimens in our cases showed eosinophils. In series of confirmed cases in adults, the frequency of CSF abnormalities is higher than in our series, 90.5% (Lombardo and Mateos, 1961), but if probable and confirmed cases are combined, the frequency is lowered to 53.9% (Marcas Sanchez and Ordonez, 1970).
Skull Roentgenograms and Pneu-moencephalograms. Tables VI and VII indicate the number of patients in whom intracerebral calcifications were detected in plain roentgenograms of the skull, and the findings in pneumoence-phalograms with air introduced either in the lumbar subarachnoid space or directly through the brain into the ventricles.
Computed Tomography of the Brain. As has already been mentioned, cerebral computed tomography has become the most valuable diagnostic aid supporting the clinical diagnosis of cerebral cysticercosis. Nevertheless, the images cannot be considered totally
specific because other entities closely resembling cysticercosis may be confused with it in the computed tomographic scan. The lesions found in the 27 patients in whom computed tomography was carried out are summarized in Table VIII and illustrated in Figure 1 to 5. These radiographic pictures may be categorized as: 1) Cerebral edema and small ventricles, which radiographically resemble pseudotumor cerebri. This finding may appear alone or associated with cysts (Figure 1). It was found in 17 of 28 cases. 2) Cystic lesions that are only observed after contrast enhancement and may be solid or annular in the form
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LE JOURNAL CANADIEN DES SCIENCES NEUROLOGIQUES
TABLE VII: Findings in Pneumoencephalogram and Ventriculogram
GROUP 1 GROUP 2 Number of Cases Number of Cases
TABLE VIII: Findings in Cerebral Computed Tomography GROUP 1 GROUP 2
Number Number of Cases of Cases Percent
0 1 4 3 1
3 1 4 0 0
TABLE VIII: Indings in Cerebral Computed Tomography
iROUP 1
dumber )f Cases
Images suggestive of cysticercosis cysts that appear single after
contrast enhancement solid cystic (annular)
radiolucent cysts nodular calcifications and/or
micronodules with calcification Cerebral edema and small ventricles Hydrocephalus, non communicating
GROUP 2
Number of Cases Percent
7 3 5
11 16
1
30.4 13.0 21.7
47.8 69.5 4.3
Normal ventricular system Cerebral edema and small ventricles Hydrocephalus Hydrocephalus and intraventricular cysts Solitary frontal mass lesion TOTAL
Diffuse cerebral edema and collapsed ventricles, without nodular lesions
Hydrocephalus and calcified cyst within 4th ventricle
Radiolucent cysts associated with micronodules and hydrocephalus
Hydrocephalus and multiple nodular lesions
Single tumor-like cystic lesion
Figure 1 — Diffuse cerebral edema and collapsed ventricles in a seven year old child with intracranial hypertension due to cerebral cysticercosis. Onset of clinical symptoms of initial acute stage was two months earlier.
Figure 2 — Multiple cystic lesions and annular cysts appear only after the injection of contrast material in the same patient as in Figure 1.
of a 'donut' (Figure 2). 3) Radiolucent cysts that probably represent infarcts or cysticerci surrounded by cerebral edema (Figure 3). 4) Calcified cysts and microcysts, visible without enhancement (Figure 4). 5) Hydrocephalus from basal cisternal and/or ventricular obstruction. 6) Solitary tumorlike images (Figure 5).
Eleven of 28 cases in our series, studied with computed tomography several months or years after the onset of symptoms, suggested that both the clinical picture and the images demonstrated by computed tomography represent intermediate or late stages of the natural history of cerebral cysticercosis, as seen in Figures 3 to 5. However, in the remaining 17 cases in which images were detected from the beginning of the course, fever, headache, vomiting and seizures were presenting symptoms. In this early stage, computed tomography invariably showed various degrees of
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THE CANADIAN JOURNAL OF NEUROLOGICAL SCIENCES
Figure 3 — Arrows indicate radiolucent areas (infarcts) and microcysts seen without contrast enhancement. Onset of symptoms one year earlier. Intermediate stage.
cerebral edema and normal or collapsed ventricles. If edema was severe, the characteristic lesions of cysticer-cosis were not visualized in the first studies, but only after several weeks or months, after the edema had subsided. Even at this time, the cysticercus lesions appear only after injection of contrast material as in Figures 1 and 2. We propose that as in other infectious diseases, the initial symptoms and cerebral edema could be caused by the arrival and implantation of the cysticercus in the central nervous system (primary infection). It also is probable that symptoms and signs do not occur, or that they are very mild as neurologically asymptomatic cases, in the non-parenchymatous or ventricular forms. The initial phenomenon of edema is later limited to the region of the brain around the cysticercus, permitting the demonstration by contrast enhancement of an image in the form of a ring or round mass, either annular or solid. After the focal edema resolves, the tomographic image (but not the cysticercus) fades or disappears, and only reappears if it calcifies or again becomes surrounded by a zone of cerebral edema. In one of the cases proven at surgery, the image of the cysticercal cysts had 'disappeared' and
406— NOVEMBER 1982
cysticerci are visible without contrast enhancement. They also appeared in the plain roentgenograms of the skull. Onset of clinical manifestations was five years earlier.
'reappeared' on two occasions that coincided chronologically with alternating exacerbations and remissions of intracranial hypertension.
Cysticercosis also may present in the form of an isolated tumor mass, as occurred in one of the cases proven at surgery (Figure 5).
Because of these changes, the following tomographic sequence emerges: (a) diffuse cerebral edema; (b) cystic lesions that appear with contrast enhancement; (c) disappearance of the cystic images; (d) calcification. The diagnosis of cerebral cysticercosis by means of computed tomography is only feasible in stages b and d. In an environment of high prevalence, the absence of cystic images in the computed tomogram of the brain does not completely rule out cerebral cysticercosis.
ACKNOWLEDGEMENT The authors would like to thank Dr. Lopez
Corella of the Department of Pathologic Anatomy of the National Institute of Pediatrics, D.I.F., for having made the material from autopsy available to us. We also thank Dr. Harvey B. Samat for his translation of the manuscript from Spanish.
Figure 5 — Solitary tumor-like cyst in the frontal region, resulting from a cysticercus surrounded by granulomatous tissue subsequently demonstrated in the histopathologic examination of the lesion.
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